Cytotoxic and immunological responses of fish leukocytes to nodularin exposure in vitro.
CLC cell line
cyanotoxins
cytokines
fish
immunotoxicity
nodularin
Journal
Journal of applied toxicology : JAT
ISSN: 1099-1263
Titre abrégé: J Appl Toxicol
Pays: England
ID NLM: 8109495
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
05
02
2021
received:
11
01
2021
accepted:
08
02
2021
pubmed:
25
2
2021
medline:
8
2
2022
entrez:
24
2
2021
Statut:
ppublish
Résumé
Nodularin (NOD) is a cyclic peptide released by bloom-forming toxic cyanobacteria Nodularia spumigena commonly occurring in brackish waters throughout the world. Although its hepatotoxic effects are well known, other negative effects of NOD have not yet been completely elucidated. The present study aims were to evaluate and compare the cytotoxic and immunotoxic effects of the toxin on primary leukocytes (from head kidney [HK]) and stable fish leukocytes (carp leucocyte cell line [CLC] cells). The cells were incubated with the cyanotoxin at concentrations of 0.001, 0.01, 0.05, or 0.1 μg/ml. After 24 h of exposure, the concentrations ≥0.05 μg/ml of toxin resulted in cytotoxicity in the primary cells, while in CLC cells, the toxic effect was obtained only with the highest concentration. Similarly, depending on the concentration, exposure to NOD causes a significant inhibition of chemotaxis of the phagocytic abilities of primary leukocytes and a significant reduction in the proliferation of lymphocytes isolated from the HKs. Moreover, CLC cells and HK leukocytes incubated with this toxin at all the mentioned concentrations showed an increased production of reactive oxygen and nitrogen species. NOD also evidently influenced the expression of genes of cytokine TNF-α and IL-10 and, to a minor extent, IL-1β and TGF-β. Notably, the observed changes in the mRNA levels of cytokines in NOD-exposed cells were evident, but not clearly dose-dependent. Interestingly, NOD did not affect the production and release of IL-1β of the CLC cells. This study provides evidence that NOD may exert cytotoxicity and immune-toxicity effects depending on cell type and toxin concentration.
Substances chimiques
Bacterial Toxins
0
Cytotoxins
0
Peptides, Cyclic
0
nodularin
0979BIK2QU
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1660-1672Informations de copyright
© 2021 John Wiley & Sons, Ltd.
Références
Andersen, R. J., Luu, H. A., Chen, D. Z. X., Holms, C. F. B., Kent, M. L., Le Blanc, M., … Williams, D. E. (1993). Chemical and biological evidence links microcystins to salmon netpen liver disease. Toxicon, 31(10), 1315-1323. https://doi.org/10.1016/0041-0101(93)90404-7
Beattie, K. A., Kaya, K., & Codd, G. A. (2000). The cyanobacterium Nodularia in PCC 7804, of freshwater origin, produces L-Har(2) nodularin. Phytochemistry, 54, 57-61. https://doi.org/10.1016/S0031-9422(00)00045-5
Chen, Y., Shen, D., & Fang, D. (2013). Nodularins in poisoning. Clinica Chimica Acta, 425, 18-29. https://doi.org/10.1016/j.cca.2013.07.005
Codd, G. A., Morrison, L. F., & Metcalf, J. S. (2005). Cyanobacterial toxins: Risk, management for health protection. Toxicology and Applied Pharmacology, 203, 264-272. https://doi.org/10.1016/j.taap.2004.02.016
Dinarello, C. A. (2018). Introduction to the interleukin-1 family of cytokines and receptors: Drivers of innate inflammation and acquired immunity. Immunological Reviews, 281(1), 5-7. https://doi.org/10.1111/imr.12624
Edler, L., Fernoe, S., Lind, M. G., Lundberg, R., & Nilsson, P. O. (1985). Mortality of dogs associated with a bloom of the cyanobacterium Nodularia spumigena in the Baltic Sea. Ophelia, 24, 103-109. https://doi.org/10.1080/00785236.1985.10426623
Edwards, C., Graham, D., Fowler, N., & Lawton, L. A. (2008). Biodegradation of microcystins and nodularin in freshwaters. Chemosphere, 73(8), 1315-1321. https://doi.org/10.1016/j.chemosphere.2008.07.015
Faltermann, S., Prétôt, R., Pernthaler, J., & Fent, K. (2016). Comparative effects of nodularin and microcystin-LR in zebrafish: 1. Uptake by organic anion transporting polypeptide Oatp 1d1 (Slco 1d1). Aquatic Toxicology, 171, 69-76. https://doi.org/10.1016/j.aquatox.2015.11.016
Fladmark, K. E., Serres, M. H., Larsen, N. L., Yasumoto, T., Aune, T., & Døskeland, S. O. (1998). Sensitive detection of apoptogenic toxins in suspension cultures of rat and salmon hepatocytes. Toxicon, 36(1), 1101-1114. https://doi.org/10.1016/S0041-0101(98)00083-X
Francis, G. (1878). Poisonous Australian lake. Nature, 18, 11-12. https://doi.org/10.1038/018011d0
Fujiki, H., & Suganuma, M. (2011). Tumor promoters-Microcystin-LR, nodularin and TNF-α and human cancer development. Anti-Cancer Agents in Medicinal Chemistry, 11(1), 4-18. https://doi.org/10.2174/187152011794941163
Harada, K.-I., Tsuji, K., Watanabe, M. F., & Kondo, F. (1996). Stability of microcystins from cyanobacteria-III. Effect of pH and temperature. Phycologia, 35(6 Suppl), 83-88. https://doi.org/10.1016/S0041-0101(96)00223-1
Harding, W. R., Rowe, N., Wessels, J. C., Beattie, K. A., & Codd, G. A. (1995). Death of a dog attributed to the cyanobacterial (blue-green algal) hepatotoxin nodularin in South Africa. Journal of the South African Veterinary Association, 66, 256-259.
Hotamisligil, G. S. (2017). Foundations of immunometabolism and implications for metabolic health and disease. Immunity, 47(3), 406-420. https://doi.org/10.1016/j.immuni.2017.08.009
Ibelings, B. W., Backer, L. C., Kardinaal, W. E. A., & Chorus, I. (2014). Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae, 40, 63-74. https://doi.org/10.1016/j.hal.2014.10.002
Kany, S., Vollrath, J. T., & Relja, B. (2019). Cytokines in inflammatory disease. International Journal of Molecular Sciences, 20(23), 6008. https://doi.org/10.3390/ijms20236008
Karjalainen, M., Kozlowsky-Suzuki, B., Lehtiniemi, M., Engström-Öst, J., Kankaanpää, H., & Viitasalo, M. (2006). Nodularin accumulation during cyanobacterial blooms and experimental depuration in zooplankton. Marine Biology, 148, 683-691. https://doi.org/10.1007/s00227-005-0126-y
Karjalainen, M., Pääkkönen, J. P., Peltonen, H., Sipiä, V., Valtonen, T., & Viitasalo, M. (2008). Nodularin concentrations in Baltic Sea zooplankton and fish during a cyanobacterial bloom. Marine Biology, 155, 483-491. https://doi.org/10.1007/s00227-008-1046-4
Karlsson, K., Sipiä, V., Kankaanpää, H., & Meriluoto, J. (2003). Mass spectrometric detection of nodularin and desmethylnodularin in mussels and flounders. Journal of Chromatography B, 784, 243-253. https://doi.org/10.1016/S1570-0232(02)00802-4
Kesarwani, P., Murali, A. K., Al-Khami, A. A., & Mehrotra, S. (2013). Redox regulation of T-cell function: From molecular mechanisms to significance in human health and disease. Antioxidants and Redox Signaling, 18(12), 1497-1534. https://doi.org/10.1089/ars.2011.4073
Lahti, K., Rapala, J., Färdig, M., Niemelä, M., & Sivonen, K. (1997). Persistence of cyanobacterial hepatotoxin microcystin-LR, in particulate material and dissolved in lake water. Water Research, 31(5), 1005-1012. https://doi.org/10.1016/S0043-1354(96)00353-3
Lehtimaki, J., Lyra, C., Suomalainen, S., Sundman, P., Rouhiainen, L., Paulin, L., … Sivonen, K. (2000). Characterization of Nodularia strains, cyanobacteria from brackish waters, by genotypic and phenotypic methods. International Journal of Systematic and Evolutionary Microbiology, 50, 1043-1053. https://doi.org/10.1099/00207713-50-3-1043
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Maatouk, I., Bouaїcha, N., Plessis, M. J., & Périn, F. (2004). Detection by 32P-postlabelling of 8-oxo-7,8-dihydro-2′-deoxyguanosine in DNA as biomarker of microcystin-LR- and nodularin-induced DNA damage in vitro in primary cultured rat hepatocytes and in vivo in rat liver. Mutation Research, 564(1), 9-20. https://doi.org/10.1016/j.mrgentox.2004.06.010
Main, D. C., Berry, P. H., Peet, R. L., & Robertson, J. P. (2008). Sheep mortalities associated with the blue green alga: Nodularia spumigena. Australian Veterinary Journal, 53, 578-581. https://doi.org/10.1111/j.1751-0813.1977.tb15830.x
Mazur-Marzec, H., Sutryk, K., Kobos, J., Hebel, A., Hohlfeld, N., Błaszczyk, A., … Jasser, I. (2013). Occurrence of cyanobacteria and cyanotoxin in the southern Baltic proper. Filamentous cyanobacteria versus single-celled picocyanobacteria. Hydrobiologia, 701, 235-252. https://doi.org/10.1007/s10750-012-1278-7
Mazur-Marzec, H., Tyminska, A., Szafranek, J., & Plinski, M. (2007). Accumulation of nodularin in sediments, mussels, and fish from the Gulf of Gdansk, southern Baltic Sea. Environmental Toxicology, 22, 101-111. https://doi.org/10.1002/tox.20239
Mishra, P., & Chan, D. C. (2016). Metabolic regulation of mitochondrial dynamics. Journal of Cell Biology, 212(4), 379-387. https://doi.org/10.1083/jcb.201511036
Moffitt, M. C., & Neilan, B. A. (2004). Characterization of the nodularin synthetase gene cluster and proposed theory of the evolution of cyanobacterial hepatotoxins. Applied and Environmental Microbiology, 70(11), 6353-6362. https://doi.org/10.1128/aem.70.11.6353-6362.2004
Nehring, S. (1993). Mortality of dogs associated with a mass development of Nodularia spumigena (Cyanophyceae) in a brackish lake at the German North Sea coast. Journal of Plankton Research, 15, 867-872. https://doi.org/10.1093/plankt/15.7.867
Parce, E. L., & Pearce, E. J. (2013). Metabolic pathways in immune cell activation and quiescence. Immunity, 38, 633-643. https://doi.org/10.1016/j.immuni.2013.04.005
Pavagadhia, S., & Balasubramanian, R. (2013). Toxicological evaluation of microcystins in aquatic fish species: Current knowledge and future directions. Aquatic Toxicology, 142-143, 1-16. https://doi.org/10.1016/j.aquatox.2013.07.010
Persson, P. E., Sivonen, K., Keto, J., Kononen, K., Niemi, M., & Viljamaa, H. (1984). Potentially toxic blue-green algae (cyanobacteria) in Finnish natural waters. Aqua Fennica, 14, 147-154.
Rymuszka, A., & Adaszek, Ł. (2012). Pro- and anti-inflammatory cytokine expression in carp blood and head kidney leukocytes exposed to cyanotoxin stress-An in vitro study. Fish ąnd Shellfish Immunology, 33, 382-388. https://doi.org/10.1016/j.fsi.2012.05.021
Rymuszka, A., & Sieroslawska, A. (2018). Comparative studies on the cytotoxic effects induced by nodularin in primary carp leukocytes and the cells of the fish CLC line. Toxicon, 148, 7-15. https://doi.org/10.1016/j.toxicon.2018.04.001
Sipiä, V., Kankaanpää, H., Peltonen, H., Vinni, M., & Meriluoto, J. (2007). Transfer of nodularin to three-spined stickleback (Gasterosteus aculeatus L.), herring, (Clupea harengus L.), and salmon (Salmo salar L.) in the northern Baltic Sea. Ecotoxicology and Environmental Safety, 66, 421-425. https://doi.org/10.1016/j.ecoenv.2006.02.006
Sipiä, V. O., Kankaanpää, H. T., Flinkman, J., Lahti, K., & Meriluoto, J. A. O. (2001). Time-dependent accumulation of cyanobacterial hepatotoxins in flounders (Platichthys flesus) and mussels (Mytilus edulis) from the northern Baltic Sea. Environmental Toxicology, 16(4), 330-336. https://doi.org/10.1002/tox.1040
Sipiä, V. O., Kankaanpää, H. T., Pflugmacher, S., Flinkman, J., Furey, A., & James, K. J. (2002). Bioaccumulation and detoxication of nodularin in tissues of flounder (Platichthys flesus), mussels (Mytilus edulis, Dreissena polymorpha), and clams (Macoma balthica) from the northern Baltic Sea. Ecotoxicology and Environmental Safety, 53, 305-311. https://doi.org/10.1006/eesa.2002.2222
Sivonen, K., Kononen, K., Carmichael, W. W., Dahlem, A. M., Rinehart, K. L., Kiviranta, J., & Niemela, S. I. (1989). Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Applied and Environmental Microbiology, 55(8), 1990-1995. https://doi.org/10.1128/aem.55.8.1990-1995.1989
Sotton, B., Domaizon, I., Anneville, O., Cattane'o, F., & Guillard, J. (2015). Nodularin and cylindrospermopsin: A review of their effects on fish. Reviews in Fish Biology and Fisheries, 25, 1-19. https://doi.org/10.1007/s11160-014-9366-6
Spinelli, J. B., & Haigis, M. C. (2018). The multifaceted contributions of mitochondria to cellular metabolism. Nature Cell Biology, 20(7), 745-754. https://doi.org/10.1038/s41556-018-0124-1
Svircĕv, Z., Lalić, D., Savić, G. B., Tokodi, N., Backovic, D. D., Chen, L., … Codd, G. A. (2019). Global geographical and historical overview of cyanotoxins distribution and cyanobacterial poisonings. Archives of Toxicology, 93, 2429-2481. https://doi.org/10.1007/s00204-019-02524-4
Tsuji, K., Naito, S., Kondo, F., Ishikawa, N., Watanabe, M. F., Suzuki, S., … Harada, K.-I. (1994). Stability of microcystins from cyanobacteria: Effect of light on decomposition and isomerisation. Environmental Science and Technology, 28, 173-177. https://doi.org/10.1021/es00050a024
Van Apeldoorn, M. E., van Egmond, H. P., Speijers, G. J. A., & Bakker, G. J. I. (2007). Toxins of cyanobacteria. Molecular Nutrition and Food Research, 51, 7-60. https://doi.org/10.1002/mnfr.200600185
Weinberg, S. E., Sena, L. A., & Chandel, N. S. (2015). Mitochondria in the regulation of innate and adaptive immunity. Immunity, 42, 406-417. https://doi.org/10.1016/j.immuni.2015.02.002
West, A. P., Brodsky, I. E., Rahner, C., Woo, D. K., Erdjument-Bromage, H., Tempst, P., … Ghosh, S. (2011). TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature, 472, 476-480. https://doi.org/10.1038/nature09973
Zhang, H., Shao, D., Wu, Y., Cai, C., Hu, C., Shou, X., … Jia, X. (2012). Apoptotic responses of Carassius auratus lymphocytes to nodularin exposure in vitro. Fish ąnd Shellfish Immunology, 33, 1229-1237. https://doi.org/10.1016/j.fsi.2012.08.016
Zhang, H., Shao, D., Wu, Y., Dai, B., Cai, C., Fang, W., … Jia, X. (2013). Regulation of nodularin-induced apoptosis by epigallocatechin-3-gallate on fish lymphocytes in vitro. Fish ąnd Shellfish Immunology, 34, 1085-1093. https://doi.org/10.1016/j.fsi.2013.01.012
Zou, J., & Secombes, C. J. (2016). The function of fish cytokines. Biology, 5(2), 23. https://doi.org/10.3390/biology5020023